Primary afferent terminals in spinal cord express presynaptic AMPA receptors

Journal of Neuroscience

Volumn 22, Issue 21, 2002, Pages 9522-9529

  Lu, Chun Rong ^a   Hwang, Se Jin ^a   Phend, Kristen D ^a   Rustioni, Aldo ^a   Valtschanoff, Juli G ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Autoreceptors; Dorsal horn; Dorsal root ganglion; Glutamate receptors; Primary afferent depolarization; Synaptic modulation

Indexed keywords

4 AMINOBUTYRIC ACID; AMPA RECEPTOR; CALCITONIN GENE RELATED PEPTIDE RECEPTOR; CHOLERA TOXIN; GLUTAMATE RECEPTOR; GLUTAMATE RECEPTOR 2; GLUTAMATE RECEPTOR 3; GLUTAMATE RECEPTOR 4; POSTSYNAPTIC RECEPTOR; PRESYNAPTIC RECEPTOR; PROTEIN SUBUNIT; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE SPINDLE AFFERENT NERVE; MYELINATED NERVE; NEUROTRANSMITTER RELEASE; NONHUMAN; NONMYELINATED NERVE; PRESYNAPTIC NERVE; PRIMARY AFFERENT DEPOLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SCIATIC NERVE; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL GANGLION;

EID: 0036849770     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-21-09522.2002     Document Type: Article

References (68)

1. Agrawal SG, Evans RH (1986) The primary afferent depolarizing action of kainate in the rat. Br J Pharmacol 87:345-355.
2. Ault B, Hildebrand LM (1993) Activation of nociceptive reflexes by peripheral kainate receptors. J Pharmacol Exp Ther 265:927-932.
3. Belyantseva IA, Lewin GR (1999) Stability and plasticity of primary afferent projections following nerve regeneration and central degeneration. Eur J Neurosci 11:457-468.
4. Bureau I, Mulle C (1998) Potentiation of GABAergic synaptic transmission by AMPA receptors in mouse cerebellar stellate cells: Changes during development. J Physiol (Lond) 509:817-831.
5. 2+ imaging reveals neurotransmitter receptors for glutamate in taste receptor cells. J Neurosci 20:7978-7985.
6. Carlton SM, Coggeshall RE (1999) Inflammation-induced changes in peripheral glutamate receptor populations. Brain Res 820:63-70.
7. Carlton SM, Hargett GL, Coggeshall RE (1995) Localization and activation of glutamate receptors in unmyelinated axons of rat glabrous skin. Neurosci Lett 197:25-28.
8. Carlton SM, Hargett GL, Coggeshall RE (1998) Plasticity in alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor subunits in the rat dorsal horn following deafferentation. Neurosci Lett 242:21-24.
9. Casado M, Dieudonne S, Ascher P (2000) Presynaptic N-methyl-D-aspartate receptors at the parallel fiber-Purkinje cell synapse. Proc Natl Acad Sci USA 97:11593-11597.
10. Caterina MJ, Julius D (2001) The vanilloid receptor: A molecular gateway to the pain pathway. Annu Rev Neurosci 24:487-517.
11. Chambille I, Rampin O (2002) AMPA glutamatergic receptor-immunoreactive subunits are expressed in lumbosacral neurons of the spinal cord and neurons of the dorsal root and pelvic ganglia controlling pelvic functions in the rat. Brain Res 933:66-80.
12. Chittajallu R, Vignes M, Dev KK, Barnes JM, Collingridge GL, Henley JM (1996) Regulation of glutamate release by presynaptic kainate receptors in the hippocampus. Nature 379:78-81.
13. Coggeshall RE, Carlton SM (1998) Ultrastructural analysis of NMDA, AMPA, and kainate receptors on unmyelinated and myelinated axons in the periphery. J Comp Neurol 391:78-86.
14. Cossart R, Tyzio R, Dinocourt C, Esclapez M, Hirsch JC, Ben-Ari Y, Bernard C (2001) Presynaptic kainate receptors that enhance the release of GABA on CA1 hippocampal interneurons. Neuron 29:497-508.
15. Davidson EM, Carlton SM (1998) Intraplantar injection of dextrophan, ketamine or memantine attenuates formalin-induced behaviors. Brain Res 785:136-142.
16. Davies J, Evans RH, Francis AA, Watkins JC (1979) Excitatory amino acid receptors and synaptic excitation in the mammalian central nervous system. J Physiol (Lond) 75:641-654.
17. Du J, Koltzenburg M, Carlton SM (2001) Glutamate-induced excitation and sensitization of nociceptors in rat glabrous skin. Pain 89:187-198.
18. Fabian-Fine R, Volknandt W, Fine A, Stewart MG (2000) Age-dependent pre- and postsynaptic distribution of AMPA receptors at synapses in CA3 stratum radiatum of hippocampal slice cultures compared with intact brain. Eur J Neurosci 12:3687-3700.
19. Friedman D, Strowbridge BW (2000) Functional role of NMDA autoreceptors in olfactory mitral cells. J Neurophysiol 84:39-50.
20. Fujimura M, Hancock MB, Cooper CW, Reumont K, Greely GH, Thompson JC (1985) Immunocytochemical localization of calcitonin gene-related peptide in pancreatic islet cells of the rat. Gastroenterology 88:1390.
21. Ginsberg SD, Price DL, Blackstone CD, Huganir RL, Martin LJ (1995) The AMPA glutamate receptor GluR3 is enriched in oxytocinergic magnocellular neurons and is localized at synapses. Neuroscience 65:563-575.
22. Glitsch M, Marty A (1999) Presynaptic effects of NMDA in cerebellar Purkinje cells and interneurons. J Neurosci 19:511-519.
23. Haydon PG (2001) Glia: Listening and talking to the synapse. Nat Rev Neurosci 2:185-193.
24. Huettner JE (1990) Glutamate receptor channels in rat DRG neurons: Activation by kainate and quisqualate and blockade of desensitization by Con A. Neuron 5:255-266.
25. Hunt SP, Mantyh PW (2001) The molecular dynamics of pain control. Nat Rev Neurosci 2:83-91.
26. Hwang SJ, Pagliardini S, Rustioni A, Valtschanoff JG (2001a) Presynaptic kainate receptors in primary afferents to the superficial laminae of the rat spinal cord. J Comp Neurol 436:275-289.
27. Hwang SJ, Rustioni A, Valtschanoff JG (2001b) Kainate receptors in primary afferents to the rat gracile nucleus. Neurosci Lett 312:137-140.
28. Jia H, Rustioni A, Valtschanoff JG (1999) Metabotropic glutamate receptors in superficial laminae of the rat dorsal horn. J Comp Neurol 410:627-642.
29. Jonas P, Burnashev N (1995) Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels. Neuron 15:987-990.
30. Kerchner GA, Wilding TJ, Li P, Zhuo M, Huettner JE (2001) Presynaptic kainate receptors regulate spinal sensory transmission. J Neurosci 21:59-66.
31. Khack BS, Henderson G (2000) Modulation of fast synaptic transmission by presynaptic ligand-gated cation channels. J Auton Nerv Syst 81:110-121.
32. Kinkelin I, Bröcker EB, Koltzenburg M, Carlton SM (2000) Localization of ionotropic glutamate receptors in peripheral axons of human skin. Neurosci Lett 283:149-152.
33. Lawand NB, Willis WD, Westlund KN (1997) Excitatory amino acid receptor involvement in peripheral nociceptive transmission in rats. Eur J Pharmacol 324:169-177.
34. Lee CJ, Engelman HS, MacDermott AB (1999) Activation of kainate receptors on rat sensory neurons evokes action potential firing and may modulate transmitter release. Ann NY Acad Sci 868:546-549.
35. Lee CJ, Bardoni R, Tong CK, Engelman HS, Joseph DJ, MacDermott AB (2002) Functional expression of AMPA receptors on central terminals of rat dorsal root ganglion neurons and presynaptic inhibition of glutamate release. Neuron 35:135-146.
36. Liu H, Wang H, Sheng M, Jan LY, Jan YN, Basbaum AI (1994) Evidence for presynaptic N-methyl-D-aspartate autoreceptors in the spinal cord dorsal horn. Proc Natl Acad Sci USA 91:8383-8387.
37. Liu H, Mantyh PW, Basbaum AI (1997) NMDA-receptor regulation of substance P release from primary afferent nociceptors. Nature 386:721-724.
38. Marvizón JCG, McRoberts JA, Ennes HS, Song B, Wang X, Jinton L, Corneliussen B, Mayer EA (2002) Two N-methyl-D-aspartate receptors in rat dorsal root ganglia with different subunit composition and localization. J Comp Neurol 446:325-341.
39. Matsubara A, Laake JH, Davanger S, Usami S, Ottersen OP (1996) Organization of AMPA receptor subunits at a glutamate synapse: A quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J Neurosci 16:4457-4467.
40. McDermott AB, Role LW, Siegelbaum SA (1999) Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22:443-485.
41. Meir A, Ginsburg S, Butkevich A, Kachalsky SG, Kaiserman I, Ahdut R, Demirgoren S, Rahamimoff R (1999) Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol Rev 79:1019-1088.
42. Paquet M, Smith Y (2000) Presynaptic NMDA receptor subunit immunoreactivity in GABAergic terminals in rat brain. J Comp Neurol 423:330-347.
43. Partin KM, Patneau DK, Winters CA, Mayer ML, Buonanno A (1993) Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 11:1069-1082.
44. Patel DR, Young AM, Croucher MJ (2001) Presynaptic α-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptor-mediated stimulation of glutamate and GABA release in the rat striatum in vivo: A dual-label microdialysis study. Neuroscience 102:101-111.
45. Peng Y-W, Blackstone CD, Huganir RL, Yau K-W (1995) Distribution of glutamate receptor subtypes in the vertebrate retina. Neuroscience 66:483-497.
46. Petralia RS, Yokotani N, Wenthold RJ (1994) Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J Neurosci 14:667-696.
47. Petralia RS, Wang Y-X, Mayat E, Wenthold RJ (1997) Glutamate receptor subunit 2-selective antibody shows a differential distribution of calcium-impermeable AMPA receptors among populations of neurons. J Comp Neurol 385:456-476.
48. Petralia RS, Sans M, Vissel B, Wang Y-X, Royle GA, Noben-Trauth K, Heinemann SF, Wenthold RJ (2001) Distribution of glutamate receptors in mice lacking the AMPA receptor subunit, GluR2. Soc Neurosci Abstr 27:481.7.
49. Picaud S, Larsson HP, Wellis DP, Lecar H, Werblin F (1995) Cone photoreceptors respond to their own glutamate release in the tiger salamander. Proc Natl Acad Sci USA 92:9417-9421.
50. Pittaluga A, Bonfanti A, Raiteri M (1997) Differential desensitization of ionotropic non-NMDA receptors having distinct neuronal location and function. Naunyn Schmiedebergs Arch Pharmacol 356:29-38.
51. Raiteri M, Garrone B, Pittaluga A (1992) N-methyl-D-aspartic acid (NMDA) and non-NMDA receptors regulating hippocampal norepinephrine release. II. Evidence for functional cooperation and for coexistence on the same axon terminal. J Pharmacol Exp Ther 260:238-242.
52. Ribeiro-da-Silva A, Coimbra A (1982) Two types of synaptic glomeruli and their distribution in laminae I-III of the rat spinal cord. J Comp Neurol 209:176-186.
53. Satake S, Saitow F, Yamada J, Konishi S (2000) Synaptic activation of AMPA receptors inhibits GABA release from cerebellar interneurons. Nat Neurosci 3:551-558.
54. Sato K, Kiyama H, Park HT, Tohyama M (1993) AMPA, KA and NMDA receptors are expressed in the rat DRG neurones. NeuroReport 4:1263-1265.
55. Schmitz D, Mellor J, Nicoll RA (2001) Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291:1972-1976.
56. Shigemoto R, Ohishi H, Nakanishi S, Mizuno N (1992) Expression of the mRNA for the rat NMDA receptor (NMDAR1) in the sensory and autonomic ganglion neurons. Neurosci Lett 144:229-232.
57. Siegel SJ, Janssen WG, Tullai JW, Rogers SW, Moran T, Heinemann SF, Morrison JH (1995) Distribution of the excitatory amino acid receptor subunits GluR2(4) in monkey hippocampus and colocalization with subunits GluR5-7 and NMDAR1. J Neurosci 15:2707-2719.
58. Smirnova T, Laroche S, Errington ML, Hicks AA, Bliss TV, Mallet J (1993) Transsynaptic expression of a presynaptic glutamate receptor during hippocampal long-term potentiation. Science 262:433-436.
59. 4-positive and -negative nociceptors are functionally distinct. J Neurosci 19:6497-6505.
60. Tachibana M, Wenthold RJ, Morioka H, Petralia RS (1994) Light and electron microscopic immunocytochemical localization of AMPA-selective glutamate receptors in the rat spinal cord. J Comp Neurol 344:431-454.
61. Valtschanoff JG, Phend KD, Bernardi PS, Weinberg RJ, Rustioni A (1994) Amino acid immunocytochemistry of primary afferent terminals in the rat dorsal horn. J Comp Neurol 346:237-252.
62. Vulchanova L, Olson TH, Stone LS, Riedl MS, Elde R, Honda CN (2001) Cytotoxic targeting of isolectin IB4-binding sensory neurons. Neuroscience 108:143-155.
63. Watanabe M, Mishina M, Inoue Y (1994) Distinct gene expression of the N-methyl-D-aspartate receptor channel subunit in peripheral neurons of the mouse sensory ganglia and adrenal gland. Neurosci Lett 165:183-186.
64. Wenthold RJ, Yokotani N, Doi K, Wada K (1992) Immunocytochemical characterization of the non-NMDA glutamate receptors subunit-specific antibodies: Evidence for a hetero-oligomeric structure in rat brain. J Biol Chem 267:501-507.
65. Westbtbrrook GL, Lothman EW (1983) Cellular and synaptic basis of kainic acid-induced hippocampal epileptiform activity. Brain Res 273:97-109.
66. Willis Jr WD, Coggeshall ER (1991) Sensory Mechanisms of the spinal Cord. New York: Plenum.
67. Woodbury JC, Ritter AM, Koerber HR (2000) On the problem of lamination in the superficial dorsal horn of mammals: A reappraisal of the substantia gelatinosa in postnatal life. J Comp Neurol 417:88-102.
68. Ye Z, Westlund KN (1996) Ultrastructural localization of glutamate receptor subunits (NMDAR1, AMPA GluR1 and GluR2/3) and spinothalamic tract cells. NeuroReport 7:2581-2585.